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Rhodoliths and Rhodolith Beds
Michael S. Foster, Gilberto M. Amado Filho, Nicholas A. Kamenos,
Rafael Riosmena-­Rodríguez, and Diana L. Steller
ABSTRACT. Rhodolith (maërl) beds, communities dominated by free living coralline algae, are
a common feature of subtidal environments worldwide. Well preserved as fossils, they have long
been recognized as important carbonate producers and paleoenvironmental indicators. Coralline
algae produce growth bands with a morphology and chemistry that record environmental variation. Rhodoliths are hard but often fragile, and growth rates are only on the order of mm/yr. The
hard, complex structure of living beds provides habitats for numerous associated species not found
on otherwise entirely sedimentary bottoms. Beds are degraded locally by dredging and other anthropogenic disturbances, and recovery is slow. They will likely suffer severe impacts worldwide
from the increasing acidity of the ocean. Investigations of rhodolith beds with scuba have enabled
precise stratified sampling that has shown the importance of individual rhodoliths as hot spots of
diversity. Observations, collections, and experiments by divers have revolutionized taxonomic studies by allowing comprehensive, detailed collection and by showing the large effects of the environment on rhodolith morphology. Facilitated by in situ collection and calibrations, corallines are now
contributing to paleoclimatic reconstructions over a broad range of temporal and spatial scales.
Beds are particularly abundant in the mesophotic zone of the Brazilian shelf where technical diving
has revealed new associations and species. This paper reviews selected past and present research on
rhodoliths and rhodolith beds that has been greatly facilitated by the use of scuba.
Michael S. Foster, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, California 95039, USA. Gilberto M.
Amado Filho, Instituto de Pesquisas, Jardim
Botânico do Rio Janeiro, Rua Pacheco Leão
915, 22460-­30, Rio de Janeiro, Brazil. Nicholas A. Kamenos, School of Geographical and
Earth Sciences, Gregory Building, University of
Glasgow, Glasgow, G12 8QQ, Scotland. Rafael
Riosmena-­Rodríguez, Programa de Investigacíon
en Botaníca Marina, Departamento de Biologia
Marina, Universidad Autónoma de Baja California Sur, Apartado postal 19-­B, La Paz, B.C.S.
23080, Mexico. ­Diana L. Steller, Moss Landing
Marine Laboratories, 8272 Moss Landing Road,
Moss Landing, California 95039, USA. Correspondence: Michael S. Foster, foster@mlml
.calstate.edu.
Manuscript received 25 January 2012; accepted 5 March 2013.
INTRODUCTION
Relative to other abundant nearshore communities like kelp forests and coral reefs,
rhodolith or maërl beds have been little investigated by marine ecologists. Even in clear,
shallow water, their lack of vertical structure in the water column makes them difficult
to distinguish from entirely soft bottoms. Observed and sampled from the bottom with
scuba, however, these purple and pink fields are complex communities formed by aggregations of unattached, nongeniculate (lacking uncalcified joints) coralline algae with
individual thalli ranging in size on the order of one to tens of cm and in shape from highly
branched twigs and fans to spheres. Live individuals may be stacked a few cm deep,
often grading below into dead fragments mixed with carbonate and terrigenous sediment
(Figure 1). They provide hard habitat for numerous other marine algae that live on their
surfaces, and for invertebrates living on and in the rhodoliths and surrounding sediments
(see the “Rhodolith Systems: Communities and Conservation” section in this paper).
There are few descriptive or experimental data to characterize the environmental
conditions that lead to rhodolith bed formation and persistence. It does appear that beds
are generally found on fairly level bottoms where light is sufficient for growth and water
motion and bioturbation are sufficient to prevent burial and anoxia from sedimentation and to move the rhodoliths. High water motion, however, can inhibit bed formation by transporting individuals out of otherwise suitable habitat or causing mechanical
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FIGURE 1. Rhodolith beds around Isla El Requéson, Baja California Sur, Mexico.
Aerial shot: Dense aggregations of rhodoliths appear as dark ribbons and occur to
a depth of 12 m. The island is 100 m across at widest point. The wide gray diagonal
bar in lower right is the airplane wing strut (photo by M. S. Foster). In situ photo:
spherical Lithophyllum margaritae rhodoliths at a depth of 6 m; diameters are
4–5 cm (photo by D. L. Steller). Core cylinder photo: Core taken through the bed
at depth of 6 m. Note stratification, with living plants at the surface grading into
dead fragments and fine sediment below; diameter = 9 cm (photo by D. L. Steller).
destruction (reviewed in Foster, 2001). These conditions can result in free-­living individuals of other organisms such as corals
and bryozoans co-­occurring with rhodoliths (e.g., James et al.,
2006). Once thought to be primarily subtropical, they are now
known to occur from tropical to polar waters and from the low
intertidal zone to 150 m deep (Bosence, 1983; Foster, 2001).
Our understanding of rhodoliths and rhodolith beds has
grown from a synergy between geologists and biologists. Geologists were the first to become interested in rhodoliths, albeit dead
ones, because these corallines are well preserved in the fossil record. At least since Darwin’s (1844) observations of rhodoliths
(“nullipores”) in calcareous strata in the Cape Verde Archipelago, rhodolith deposits have been used to interpret geological
change and paleoenvironments (e.g., Bassi et al., 2009). Early
ecological work on live beds was pursued in the intertidal zone,
or subtidally with dredges or grabs, and was focused on species
composition and natural history (e.g., Weber-­van Bosse and Foslie, 1904). In contrast to attached organisms on hard bottoms,
dredging in rhodolith beds can provide good samples of the
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organisms present. This method is still being used to locate beds
and their boundaries (e.g., Foster et al., 1997), especially over
large areas where scuba is inefficient and acoustical mapping
equipment (e.g., Ehrhold et al., 2006) is not available. Dredging can be effective for species information and mapping, but
as in other shallow-­water habitats, observation of microhabitat
distribution and use, studies of processes, and field experimental
manipulations require scuba.
One of the first and the most comprehensive in situ studies
on rhodolith systems was by Bosence (1976), a geologist interested in using characteristics of living rhodoliths and rhodolith
beds to better interpret fossil deposits. Bosence (1976) carefully
mapped rhodolith distribution in a bay in Ireland, and examined the relationships between the environment (especially water
motion) and rhodolith species distribution and morphology. He
wrote the first review of rhodolith ecology (Bosence, 1983), highlighting the advantages of scuba as a research tool and providing
a foundation and stimulus for future studies that now include
the full spectrum of ecological topics and approaches, including past and present climate change. Rhodoliths are particularly
useful for the latter as they are widely distributed, grow slowly
(~mm/yr) and, like temperate trees and hermatypic corals, leave
a record of their growth as bands within the thallus (see the
“Rhodoliths as Environmental Recorders” section in this paper).
Sadly, reduced growth and dissolution caused by future changes
in ocean pH and temperature may result in the absence of bands
and the decline of rhodolith beds.
A thorough review of rhodoliths and rhodolith bed ecology
is beyond the scope of this paper. Instead, each author discusses
a current topic in his or her area of interest and expertise: Introduction (MSF), Diving to the Edge of Rhodolith Taxonomy and
Evolution (RRR), Rhodolith Communities and Conservation
(DLS), Deep Beds in Brazil (GAF), and Rhodoliths as Environmental Recorders (NAK). Investigations of these topics have all
been greatly facilitated by the use of scuba. We hope the reader
will find the discussions interesting and informative, stimulating
further interest in and study and conservation of these tumble
weeds of the sea.
DIVING TO THE EDGE OF RHODOLITH
SYSTEMATICS AND EVOLUTION
Seaweed distribution and the factors that affect it are key
scientific questions; Setchell (1893) clearly understood the importance of temperature limits to the geographic distribution of
kelp species and the importance of distribution to systematics.
The utility of such information, however, depends on the validity
of the species identification and how well collections represent
the geographic and depth distributions of species in nature. These
problems have been particularly difficult to overcome in coralline red algae (Corallinales, Rhodophyta), and especially with the
nongeniculate species that occur as rhodoliths. The characteristics
used to classify rhodoliths in the early 1700s could not segregate
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them from corals or stones (Woelkerling, 1988) and names such
as Lithophyllum are still in use for both algae and corals (Veron,
1995). After recognizing rhodoliths as calcified, photosynthetic
organisms, most investigators thought that species of Lithophyllum were characteristic of warm waters and Lithothamnium of
cold waters (Foslie, 1900). Such relationships were based on sampling and observations from the intertidal zone or on specimens
dredged from the shallow subtidal. Distributional knowledge was
further compromised by the numerous species that were described
based largely on external morphology. For example, investigators
like Mikael Foslie described 485 species and varieties (Woelkerling et al., 2005) based primarily on external morphology, at least
half of which were rhodolith-­forming species.
As a consequence of developments in underwater technology including scuba, other diving methods, and better remote
sampling devices, it soon became clear that coralline red algae
were abundant, widespread, and often a key component of the
ocean floor at depths to nearly 300 m. These developments also
dramatically increased extraction of live and dead rhodoliths
(maërl) for commercial purposes, an activity that has occurred
since the seventeenth century along French and U.K. coasts (Grall
and Hall-­Spencer, 2003; see the “Rhodolith Systems: Communities and Conservation” section in this paper).
While large rhodolith beds have long been known in the
northeast Atlantic, the surge in ocean exploration beginning in
the twentieth century revealed the presence of coralline banks
in Malaysia (Weber-­van Bosse, 1904), the Galapagos (Lemoine,
1930), the eastern Pacific (Dawson 1960a, 1960b), and Brazil,
where beds cover hundreds of square km (Kempf, 1970; see the
“Deep Beds in Brazil” section in this paper). These explorations
were followed by extensive surveys in Brazil (Lavrado, 2006)
and around the Hawaiian Islands (Adey et al., 1982). Hundreds
of species were described from deeper areas, strongly suggesting
that more species would be found as surveys continued. However, these collections were all made by dredging, and the few
specimens obtained may not have been representative of local
variation. Taxonomic analyses could be biased by describing new
species based on a limited number of specimens.
This situation greatly improved in the 1950s when E.Y.
Dawson started to use scuba for his research, diving with only
mask, fins, tank, regulator, and a very rudimentary buoyancy
compensator, with shorts and a shirt for a diving suit (Norris,
2010: figs. 7, 8). Dawson could observe and collect numerous
representative specimens under water, including what became
Porolithon castellum and Sporolithon pacificum, the latter a very
distinctive species (Dawson, 1960b). The allure of the visual record meant that underwater photography began to be used in
the early days of diving. Dawson soon added a camera to his
equipment, and his dive partner took one of the first underwater
photographs of a coralline alga. Scuba diving quickly became
part of the usual collecting approach for many researchers. It
was a boon for taxonomists, who need to collect hundreds of
individuals for rigorous morphological, anatomical, and now
molecular analyses.
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As scuba was recognized as an essential tool for marine
scientists, scientific diving facilities and training programs, both
fixed and portable, were developed around the world. There are
a number of excellent examples of the success of such facilities in
helping contribute to our knowledge of coralline taxonomy and
diversity, including the descriptions of Tenarea tesselatum (Litt­
ler, 1971) from the tropics and Ezo eppiyessoense (Adey et al.,
1974) from a temperate region. Scuba investigations continue to
discover new and interesting subtidal coralline species, including
Synarthrophyton schielianum (Woelkerling and Foster, 1989),
which has one of the strangest morphologies among the red algae.
In situ ecological studies of rhodolith-­forming species began
in the 1970s, including the seminal studies of Bosellini and Ginsburg (1971) and Bosence (1976). These studies documented the
large effects of the environment, especially variation in water
motion, on rhodolith shape and branching characteristics. The
results enlightened paleoenvironmental interpretations but also
served as a warning to taxonomists that many described rhodolith
species might be morphological variants of the same species. For
Mediterranean waters, Ballesteros (1988) wrote the first review of
rhodolith species using information obtained by diving, and Basso
(1998) critically evaluated species boundaries. Taxonomic evaluations based on scuba collections using research stations in the
western Pacific were done by Verheij (1993) in Indonesia and Ballesteros and Afonso-­Carrillo (1995) in the Indo-­Pacific. In the eastern Pacific, the diving study of Steller and Foster (1995) further
showed the influence of the environment on rhodolith morphology. This environmentally induced morphological plasticity (Figure 2) obscured the real taxonomic boundaries used for the species
until detailed anatomical work was done (Riosmena-­Rodríguez et
FIGURE 2. Growth-­form variation in the rhodolith Lithophyllum margaritae from the Gulf of California. The small rhodolith in lower left
corner is 1.5 cm wide. From Riosmena-­Rodríguez et al., 1999.
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al., 1999). Additional genetic information from Schaeffer et al.
(2002) has shown that some isolation occurs among populations.
New descriptions and studies of rhodolith beds (e.g., Harvey et
al., 2005; Konar et al., 2006) and collections and species analyses
of the rhodoliths found are helping to refine our understanding of
growth forms, species, and species distributions.
Rhodolith beds are distributed worldwide but a thorough
bathymetric evaluation has not been produced at the global
scale. Harvey and Woelkerling (2007) did an excellent review
of the rhodolith-­
forming species in the coralline algae, concluding that there are 8 genera and 71 species cited in modern
studies. Most of the records in this review came from dredging,
not scuba collection, again suggesting that more of the latter is
needed to clarify the boundaries between species. New technologies for working under water, along with the traditional methods
of ocean exploration, provide very exciting opportunities that
will contribute to understanding the evolutionary history of
rhodolith-­forming species via comparisons of subtidal findings
with the geological record of well-­preserved coralline red algae.
Collections using scuba diving and/or remotely operated
underwater vehicles (ROVs) have already provided new records
and evolutionary insights based on research occurring around
the world (e.g., Brazilian continental shelf, Farias et al., 2010,
and Bahia et al., 2011; Galician estuaries, Peña et al., 2011; Gulf
of California, Riosmena-­Rodríguez et al., 2010). In the future, it
might be particularly interesting to examine very old fossil deposits along the coast of the Bahamas where Littler et al. (1985)
described the deepest known plant life, a coralline alga. Coralline
algae originated in the Cambrian (Woelkerling, 1988) and are one
of the oldest clades in red algae. New studies will likely change
our current views on rhodolith taxonomy and systematics due to
probable discoveries of presently unknown evolutionary clades.
The current challenge with regard to rhodolith systematic
biology is to use information from field collections in combination with genetic analyses to better resolve species and answer
evolutionary questions. This needs to involve the use of nuclear,
chloroplast, and mitochondrial genes to delimit the number of
clades among rhodoliths. These genetic approaches, combined
with correlations between molecular clock and isotopic ages
from carbonate deposits, should allow the construction of a
model based on evolution and development (EVO DEVO), as
suggested by Aguirre et al. (2010). The origins and development
of rhodolith deposits can also be explored using mitochondrial
genes to determine the origins of populations and the relative importance to bed persistence of fragmentation versus recruitment
from spores. This is the edge of taxonomy and evolution, and
scuba will therefore continue to be essential to advances.
RHODOLITH SYSTEMS:
COMMUNITIES AND CONSERVATION
Individual rhodoliths, or “nodules,” can form intricately
branched structures, and large aggregations of nodules form
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beds, complex biogenic matrices of hard branches that create numerous interstitial spaces. Beds typically form as a living layer on
top of an otherwise sedimentary bottom (Figure 1) and harbor
a diverse and often unique assemblage of associated species (Cabioch, 1969; Keegan, 1974). In addition to being considered biodiversity hot spots, rhodolith beds are also settlement sites and
nursery grounds for important commercial species. Fleshy macroalgae are found on the rhodolith surfaces; invertebrates are
found among or bored into rhodolith branches (cryptofauna),
moving over and among the rhodoliths, or burrowed into underlying sediments (infauna) (Grall and Glemarec, 1997; Steller et
al., 2003). Burrowing fish add further benthic complexity, making these habitats rich sites for ecological exploration.
Rhodolith beds are generally more species rich and support
higher population densities than adjacent sedimentary habitats
(Birkett et al., 1998; Steller et al., 2003). For example, stratified
sampling of subhabitats in a rhodolith bed and a sand flat found
richness to be 1.7 times, and total abundance 900 times, greater
in a rhodolith bed than in adjacent non-­rhodolith habitat (Steller
et al., 2003). This has been attributed to the higher number of
available niches in rhodoliths relative to sand. Beds support complex food webs of predators, suspension feeders, detritivores,
and micrograzers in the eastern Atlantic (Grall et al., 2006).
Early studies using scuba were largely devoted to determining the distribution of rhodoliths and associated species (Keegan,
1974; Bosence, 1979), and such studies encouraged the development of diver-­operated sampling devices such as suction dredges
to more precisely sample soft-­bottom species (Keegan and Konnecker, 1973). This ecological community research continues as
new beds are discovered and explored, and many recent studies
have shifted their focus to understanding the mechanisms underlying ecological relationships, reflecting the evolution of ecological research as well as changes in research methods. Traditional
ship-­based benthic sampling with dredges and grabs has been
useful in establishing general patterns of distribution and diversity. Combining this type of sampling with scuba allows for (1)
efficient visual surveys of large areas, (2) more precise habitat
sampling, (3) enhanced detection of rare, seasonal, and fragile
associated species and species interactions, and (4) in situ environmental measurements and experimental manipulations. As a
result, surveys worldwide now report that the greatest contributors to high richness and abundance are cryptofauna (primarily
arthropods, annelids, and cnidarians) that increase as live cover
and rhodolith size and branching increases. Such microhabitat
associations can be obscured or eliminated in homogenized samples from dredges, grabs, and cores.
Large-­scale studies comparing species in rhodolith beds to
those in entirely sedimentary habitats have measured species
diversity of either the entire community or a dominant group
of organisms. In general, higher diversity and abundance of a
community (Grall et al., 2006), or of specific invertebrate groups
(e.g., polychaetes; Figueiredo et al., 2007), has been correlated
with higher density and cover of live rhodoliths and more complex habitat. This pattern is not consistent for all species; infauna
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such as soft-­sediment meiofaunal bivalves can be more diverse
on dead (versus live) rhodolith substrate (Jackson et al., 2004).
When rhodoliths grow as distinct, densely branched, spherical individuals (Figure 2) rather than mats of intertwined, jack-­
like structures, the richness and abundance of species in and on
them increases with rhodolith size, branching, and available space
(Steller et al., 2003; Hinojosa-­Arango and Riosmena-­Rodríguez,
2004; Foster et al., 2007). Elucidating such relationships requires
using scuba to carefully collect individual specimens, followed by
proper fixation and careful dissection. Such studies have shown
that 2–6 cm–diameter, highly branched Lithophyllum margaritae and 5–9 cm–diameter, knobby, branched Lithothamnion
muellerii from the Gulf of California can harbor 10–90 cryptofaunal species per rhodolith, with more species in larger individuals. Rhodolith densities can beupwards of 5,000–10,000 m−2
(D. Steller, personal observation), resulting in exceptionally high
cryptofaunal abundance. The most abundant taxa often include
crustaceans, polychaetes, ophiuroids, and mollusks. Collectively,
these findings support the notion that large, old individuals act
as “old-­growth rhodoliths,” and are inhabited by species such as
stomatopods and burrowing clams not found on and in smaller
rhodoliths (Foster et al., 2007).
Diving studies have also revealed rare and new species, and
some unique and interesting ecological relationships. Eight species of small (2–10 mm) cryptofaunal chitons were collected
from between the branches of Lithophyllum margaritae in the
Gulf of California, four of which were previously undescribed
(Clark, 2000). Reports of complex, fragile nests built by the mollusk Limaria hians, a gaping file shell, came from in situ observations (Hall-­Spencer et al., 2003). Macroinvertebrates such as the
urchin Toxopneustes roseus can cover themselves with rhodoliths and also prefer to eat them rather than fleshy algae (James,
2000). The burrowing crustacean Upogebia deltaura creates extensive burrows among the rhodoliths that can withstand disturbance (Hall-­Spencer and Atkinson, 1999). Such investigations
are still few but the use of standardized scuba-­enabled subtidal
sampling designs and methods (Steller et al., 2007) promises to
reveal more new species, as well as ecological and biogeographic
insights.
The productivity of rhodolith beds is enhanced by a diverse
associated flora that grows on the hard substrata they provide
(Jacquotte, 1962; Grall et al., 2006), and some algal species appear to be confined to rhodolith habitat (Leliaert et al., 2009). The
associated flora often changes seasonally, as well as with depth.
These changes are correlated with variation in rhodolith characteristics such as cover, depth, and the amount of live material. The
changes are also correlated with changing oceanographic conditions, such as water motion, which can turn and roll rhodoliths,
as well as temperature (Cabioch, 1969; Lieberman et al., 1979;
Hily et al., 1992; Birkett et al., 1998; Steller et al., 2003; Amado-­
Filho et al., 2007; Riul et al., 2009; Peña and Barbara, 2010). In
a subtropical Gulf of California bed, Steller et al. (2003) reported
up to thirty common macroalgal species in winter, but a maximum of eight species in summer. Year-­long sampling at 1½-­month
intervals has shown similar large seasonal changes in the flora of
a European Atlantic bed, as well as relationships between these
changes and the depth of the living rhodolith layer and the live/
dead rhodolith ratio (Peña and Barbara, 2010).
Qualitative in situ observations in the Gulf of California
and elsewhere suggest that the diversity of large fishes in the
water column above rhodolith beds is generally low, probably
because there is little structure above the bottom. Reports of
numerous associated water column fishes (e.g., Aburto-­Oropeza
and Balart, 2001) are likely an artifact of the beds being in close
proximity to reefs that provide macrostructure. Numerous cryptic demersal, benthic, and/or burrowing species such as gobies
and blennies are found on, in, and among rhodoliths, and juveniles of species such as cod have been reported to use rhodolith
beds as feeding areas (Hall-­Spencer et al., 2003). Large, bottom-­
dwelling or burrowing species can be quite common, including sheephead (Semicossyphus pulcher) in California, and tiger
snake eels (Myrichthys maculosus), bullseye electric (Diplobatis
ommanata) and other rays, and Cortez garden eels (Taeniconger
digueti) in the Gulf of California (D. Steller and M. Foster, pers.
obs.). The distribution of rhodolith beds appears to be largely
constrained by abiotic variables such as water motion and light,
but within-­bed structure and perhaps even bed persistence may
be strongly affected by biological interactions. Bioturbation by
invertebrates and fishes moves rhodoliths and resuspends fine
sediment, likely facilitating rhodolith growth and bed maintenance (Marrack, 1999).
Rhodolith beds may act as nursery habitat for a variety of
species. Bivalves are abundant in rhodolith beds in areas such as
Georges Bank (Thouzeau, 1991), the Gulf of California (Steller
and Caceras-­Martinez, 2009), and the eastern Atlantic (Hily et
al., 1992; Hall-­Spencer, 1998; Hall-­Spencer and Moore, 2000),
and rhodolith beds may play a role as nursery habitats for scallops. Scallop–rhodolith bed interactions have been of particular
interest because scallops are commercially harvested and their
life history is well known. Scallop larvae have been shown to
preferentially settle on living (versus dead) rhodoliths (Steller
and Caceras-­Martinez, 2009). This preference likely contributes
to high juvenile scallop densities (Kamenos et al., 2004a)h@ due
to greater scallop selection, attachment, and growth (Kamenos et
al., 2004b, 2004c). Rhodolith beds may also benefit adult scallops by providing a refuge from predation (Steller et al., 2003;
Kamenos et al., 2006). Patterns of water motion responsible for
rhodolith maintenance may also influence larval delivery of a
number of associated species, a mechanism that remains to be
investigated.
While natural disturbances are an essential feature of rhodolith ecosystems, anthropogenic disturbances can be catastrophic.
This is readily clear from diving observations made over a once-­
thriving rhodolith bed that had been crushed by a scallop dredge.
Beds have been entirely or partially destroyed by extraction of
calcareous sediment, bottom fisheries, and degraded water quality from fish farms (De Grave, 1999; Hall-­Spencer and Moore,
2000; Hall-­Spencer et al., 2006). Smaller-­scale disturbances such
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as anchoring or mooring in coastal bays also occur, but have
received less attention.
In addition to localized destruction, rhodolith beds worldwide will likely be impacted by decreasing ocean pH linked to
rising atmospheric CO2 (Kleypas et al., 2006). Coralline algae,
with their very soluble high-­Mg calcite, are predicted to be in
the first suite of species severely impacted by ocean acidification
(Kuffner et al., 2007; Jokiel et al., 2008). Chemical dissolution
could make them more susceptible to other physical and biological disturbances and decrease post-­disturbance recovery rates.
The positive relationship between biodiversity and rhodolith
density, nodule size, and branching strongly suggests that factors
negatively impacting nodule characteristics would likely lead to
negative community-­level impacts.
The need for protecting rhodolith beds from dredging,
trawling, and other relatively small-­scale disturbances has been
recognized by conservation directives in the European Union,
Australia, New Zealand, and Mexico (review in Riosmena-­
Rodríguez et al., 2010). On the largest scale, however, little progress has been made toward reducing CO2 emissions. It remains to
be seen how effective local conservation measures will be in the
face of global change.
DEEP BEDS IN BRAZIL
The Brazilian coast supports the largest known rhodolith
beds in the world, covering extensive areas of the north, northeastern, and southeastern Brazilian continental shelf (Kempf,
1970; Milliman, 1977; Amado-­Filho et al., 2007). However,
our understanding of the latitudinal distribution and community structure of these beds is still in its infancy. Many rhodolith
studies in Brazil, especially the early ones, were focused on the
characterization of shelf sediments and prospects for potential
commercial exploitation (Milliman and Amaral, 1974; Dias,
2000). Only a few published studies have considered the beds
in a biological context that includes consistent information
about meso-­and small-­scale distribution, bed structure, associated organisms, and the species composition of the rhodoliths
(e.g., Gherardi, 2004; Riul et al., 2009; Villas-­Boas et al., 2009;
Amado-­Filho et al., 2010).
These latter studies have found a high diversity of organisms
associated with rhodolith beds and highlight their ecological relevance. A general evaluation of the marine biota in the Brazilian
exclusive economic zone (the marine area extending 320 km offshore) indicated rhodolith beds increase the diversity of epibenthic organisms, with Shannon diversity indices (H’) of 4.0–5.1
found to depths of 250 m in this ecosystem (Lavrado, 2006).
These and other data obtained during the 1990s and the early
2000s were, however, based on dredging and the analyses were
largely qualitative. Most rhodolith beds in Brazil still remain unexplored or poorly known ecologically. This is largely because
the beds occur mostly in mesophotic habitats (~30–120 m depth)
that are difficult to adequately access with standard scuba.
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As pointed out by Bridge et al. (2010), information on biotic and abiotic aspects of mesophotic habitats remains extremely
scarce due to logistical and technological restrictions, particularly
when compared with shallow-­
water habitats. This is true for
rhodolith beds in Brazil, but recent advances in mixed-­gas diving techniques (Figure 3), complemented by ROV observations
and high-­resolution, multibeam, bathymetric mapping systems,
allow us to begin determining their extent, structure, and dynamics. These tools are now being used to investigate extensive areas
of the continental shelf (e.g., Abrolhos Bank), tops of seamounts
(Vitoria-­Trindade Ridge), and around oceanic islands (e.g., Trindade Island and Fernando de Noronha Island; Figure 4).
One of the most interesting features of these mesophotic
habitats, recently investigated using technical diving, are rhodolith beds inhabited by populations of the deep water endemic
kelp Laminaria abyssalis. This kelp occurs on the continental
shelf at latitudes of 19°–23° S and depths of 45–120 m where
the bottom is completely covered by rhodoliths (Amado-­Filho
et al., 2007). Kelp populations are closely associated with the
rhodoliths; all L. abyssalis holdfasts are attached to one or more
rhodoliths. Graham et al. (2007) suggested that such deep water
kelp refugia are potential hot spots of tropical marine diversity
and productivity. This suggestion has been confirmed in the Brazilian deep water rhodolith–kelp beds, as endemic species of different taxonomic groups have been cited to this area.
The northern limit of Brazilian L. abyssalis populations is
determined by the southern edge of Abrolhos Bank. The Abrolhos Shelf (16°50′S–19°45′S; Figure 4) is an ~6,000 km2 enlargement of the eastern Brazilian continental shelf, and encompasses
the largest (~325 km2) and richest reefs in the South Atlantic
(Leão and Ginsburg, 1997). These reefs are well known for their
unique coral assemblages dominated by Brazilian-­endemic, Neogene relics belonging to the genus Mussismilia. Investigations
combining side scan sonar, ROV images, and scuba diving show
that rhodolith beds are the predominant feature from north to
south across the Abrolhos Shelf at depths from ~25 m to ~110 m.
These beds are composed of at least five non-­geniculate coralline
species.
The Vitoria-­
Trindade Ridge (VTR; 20°S–21°S) is a
1,150 km east–west chain of nine seamounts in the South Atlantic that includes two small and highly isolated islands at its
eastern end (Figure 4). Previous biological sampling on the VTR
was largely restricted to (1) dredging, (2) data from commercial
fisheries, and (3) a few scientific diving operations in the shallow waters surrounding Trindade Island. The mesophotic zone
on the top of two seamounts (Davis and Jaseur) were surveyed
in March 2009 using a combination of ROVs, mixed-­gas technical dives, and a single-­beam bathymetry system. The seamounts
have predominantly flattened tops that result from alternating
periods of growth and erosion of carbonate algal deposits over
volcanic pedestals during periods of high and low sea level (Almeida, 1965). At present sea level, the flattened summits of the
seamounts are all situated in relatively shallow water, with minimum depths ranging from 40 m to 110 m. The seamount tops
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FIGURE 3. Technical diving equipment being used to take video images at 60 m on Fernando de Noronha Island
shelf, Brazil. Photo by Z. Matheus, courtesy of G. M. Amado Filho.
rise up to 50 m from the bottom, and are dominated by rhodoliths with a high diversity of associated species including seaweeds, sponges, corals, black corals, octocorals, and reef fishes.
Rhodolith beds are also the main feature surrounding Fernando
de Noronha, a typical tropical island (03°50′S, 32°25′W, about
345 km east of the coast of Brazil; Figure 4) known as the best
diving location in Brazil. These beds, found down to 120 m at the
edge of the island shelf, were also discovered using technical diving. The ongoing description and study of these unique coralline
environments will provide essential information for understanding the ecology, biodiversity, and connectivity of South Atlantic
reef communities.
RHODOLITHS AS
ENVIRONMENTAL RECORDERS
FIGURE 4. Locations of mesophotic rhodolith beds on the Brazilian
Shelf.
Coralline algae have several characteristics that make them
ideal candidates for recording the environment in which they
grow. When these algae grow, they lay down annual and subannual carbonate-­derived growth bands composed of high-­Mg
calcite (Figure 5; Henrich et al., 1996; Kamenos et al., 2008).
Groups of subannual primary growth bands resulting from variation in cell size and wall thickness can be grouped into dark
n u mber 3 9
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151
FIGURE 6. A Lithothamnion glaciale bed and associated fauna on
the west coast of Scotland. Scale = 5 cm. Photo by N. Kamenos.
FIGURE 5. Annual banding patterns in a transverse sectioned Lithothamnion glaciale branch. Scale = 1 mm. Photo by N. Kamenos.
and light pairs that form higher-­order annual banding patterns
(Freiwald and Henrich, 1994). While Lithothamnion glaciale
and Clathromorphum compactum show clear annual banding
patterns (Halfar et al., 2008; Kamenos et al., 2008), other species
such as Phymatolithon calcareum show clearer subannual banding patterns (Blake and Maggs, 2003). In some species, growth
is not hampered by prolonged periods of low temperature (e.g.,
L. glaciale; Henrich et al., 1996) or darkness (e.g., L. glaciale;
Freiwald and Henrich, 1994), while in others there is reduced
growth in winter (e.g., C. compactum; Halfar et al., 2008). As
new thalli grow at the surface of the rhodolith bed, older thalli
become covered by sediment, die, and form part of the dead deposit. Individual coralline algal thalli can live to at least ~850
years (Frantz et al., 2005) and accumulations of these algal thalli
have created maërl deposits spanning the last 20,000 years (Figure 6; Bosence, 1983). Unlike most carbonate-­depositing organisms, which have a more restricted distribution, coralline algae
occur from polar (Schwarz et al., 2005) to tropical (Littler et al.,
1991) shallow seas.
Three key steps are typically used in the development of
an environmental recorder (known as a proxy; Kamenos et al.,
2009). For coralline algae this involves the following: (1) calibration, which involves understanding the biology of the algae and
experimentally determining how growth, for example, responds
to environmental stimuli such as temperature (Kamenos et al.,
2008); (2) validation of the algae as proxies, which requires appropriate biogeochemical analyses to determine if the observed
response of the alga’s physical or chemical characteristics to environmental change are a direct response to that change or the
record of a tertiary response to a related physiological process
(Kamenos et al., 2009); and, (3) application, which establishes
that the coralline algae are recording a specific environmental
stimulus and can be used to reconstruct and understand environmental changes that occurred before the availability of instrumental records (Kamenos, 2010; Burdett et al., 2011).
Unfortunately, many proxies do not undergo this rigorous and
important three-­step process, rendering their utility questionable.
Scuba has been instrumental in the development of rhodoliths as environmental recorders. Because of their fragile nature,
hand collection is the only suitable technique for calibrating the
algae in the field or collecting them for calibration in the laboratory. Subsequent to calibration, collection of samples for paleoenvironmental reconstruction involves determination of the
most suitable sampling location (e.g., the location likely to provide the longest record) and precise manipulation of sampling
apparatus (e.g., corer placement or airlift attachment). These
tasks can only be reliably achieved using on-­site sampling via
scuba. Remote mechanical collection is not suitable due to the
absence of specific sampling location information (e.g., what was
the orientation of the surface algae on collection?). While suitable remote coring equipment can be used in softer sediments
(e.g., vibra corer), the dense nature of rhodolith deposits requires
coring techniques capable of penetrating the sediment without
causing excessive disturbance. At present, scuba is the ideal tool
for conducting such coring activities.
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Relationships between environmental parameters and
growth have been observed in coralline algae. Significant negative relationships are present between temperature and calcite
density in Lithothamnion glaciale (Kamenos and Law, 2010), as
well as temperature and growth-­band width in Clathromorphum
compactum (Halfar et al., 2011). In both species growth characteristics were correlated to decadal-­scale temperature records at
collection sites but were characterized by noticeable variability.
That variability was attributed to localized control of incident
radiation (e.g., algal blooms) and thus it is likely that growth
contains a record of both temperature and irradiance (Kamenos
and Law, 2010). This was addressed by the development of a
growth-­environment model that accounts for both temperature
and light (as photosynthetically active radiation or PAR; Burdett et al., 2011). By combining a record of summer calcification
within individual Lithothamnion glaciale growth bands with
known temperature records for the area, cloud cover (indicative
of PAR) history on the west coast of Scotland was reconstructed
that indicated a modest increase in cloud cover trends since 1910
(Burdett et al., 2011).
The chemistry of the calcite deposited by coralline algae
within their growth bands also serves as an environmental recorder. Initial observations indicated elemental concentrations
within coralline algae varied directly (Chave and Wheeler, 1965)
and indirectly (Moberly, 1968) with environmental fluctuations.
More recently, Mg concentrations within Lithothamnion glaciale
have been observed to represent ambient temperature of the seawater in which the algae grew at fortnightly resolutions (Kamenos
et al., 2008), as well as sea-­surface temperature at seasonal resolution (Halfar et al., 2000). This response allowed Lithothamion
glaciale to be validated as a paleotemperature recorder (Kamenos
et al., 2009), enabling the first biweekly resolution reconstruction
of Atlantic marine temperatures since ~1350 (Kamenos, 2010).
δ18O in Clathromorphum nereostratum and Lithothamnion glaciale represents ambient seawater temperature at seasonal resolutions and has been used to reconstruct northeastern Atlantic
sea-­surface temperature since 1970 (Halfar et al., 2000, 2008).
Lithothamnion muellerii and C. nereostratum have been shown
to record atmospheric 14C concentrations (Frantz et al., 2000,
2005), which are critical for determining long-­term growth rates
and age in coralline algae as well as dating the exact timing of climatic events recorded by the growth-­banding structure or chemistry within the algae. Overall, coralline algae are ideally suited
as chemical environmental recorders because (1) they do not suffer diagenetic effects due to the presence of the living membrane
covering the carbonate skeleton (Alexandersson, 1974); (2) there
is no stress-­related geochemical deviation in Mg/Ca–temperature
relationships (Kamenos et al., 2008); and, (3) there is no non-­
equilibrium-­
associated oxygen isotope fractionation in maërl
(Rahimpour-­Bonab et al., 1997; Halfar et al., 2007).
Scuba has played a central role in facilitating an understanding of how coralline algae act as environmental recorders
through their utility in paleoenvironmental reconstructions. With
the need for increasingly resolved spatio-­temporal paleoclimate
records to better understand recent climate trends, these algae
are beginning to receive increased attention as environmental
recorders.
CONCLUSIONS
As they have for other shallow subtidal environments, in
situ investigations using scuba have improved our understanding
of rhodoliths and rhodolith beds far beyond that achievable by
dredging and other remote research techniques. Scuba enabled
detailed sampling that continues to clarify the taxonomy and
evolutionary relationships of rhodoliths and associated species.
It has allowed the direct determination of bed distribution and
abundance patterns, and field experiments to test hypotheses
about the causes of these patterns. Such studies, including those
in deep water that use technical diving, continue to provide new
insights into bed structure and function. Careful collection and
underwater experimentation have also revealed rhodoliths to be
exceptional environmental recorders. Beds are, however, very
susceptible to disturbance and climate change. Their conservation must be a priority if we are to continue to enjoy, better understand, and learn from these remarkable communities and the
plants that dominate them.
ACKNOWLEDGMENTS
We thank the diving community for providing locations and
in situ observations of new rhodolith beds that have contributed to understanding rhodolith distribution and provided new
opportunities for research. Coauthor GAF thanks the Brazilian
research agencies CNPq, CAPES, and FAPERJ for financial support for development projects. Coauthor NK is in receipt of a
Royal Society of Edinburgh/Scottish Government Personal Research Fellowship (RSE 48704/1).
This chapter is dedicated to the memory of Isabella A. Abbott
(1919–2010), who contributed enormously to our knowledge of
marine algae, championed international scientific collaboration,
and always encouraged searches for subtidal seaweeds.
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